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Pollen Harvesting and Reproductive Rates in Specialized Solitary Bees

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Pollen Harvesting and Reproductive Rates in Specialized Solitary Bees Ann. Zool. Fennici 44: 405–414 ISSN 0003-455X (print), ISSN 1797-2450 (online) Helsinki 19 December 2007 © Finnish Zoological and Botanical Publishing Board 2007 Pollen harvesting and reproductive rates in specialized solitary bees Markus Franzén1 & Magnus Larsson2 1) Department of Animal Ecology, Lund University, Ecology Building Sölvegatan 37, SE-223 62 Lund, Sweden (e-mail: [email protected]) 2) Department of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villavägen 14, SE-752 36 Uppsala, Sweden Received 23 Jan. 2007, revised version received 29 Oct. 2007, accepted 29 Oct. 2007 Franzén, M. & Larsson, M. 2007: Pollen harvesting and reproductive rates in specialized solitary bees. — Ann. Zool. Fennici 44: 405–414. Andrena humilis is an endangered oligolectic solitary bee and has declined in recent decades throughout western Europe. The aim of this study was to explore the pollen harvesting pattern and to determine the reproductive rate in specialized andrenid bees. We measured the amount of pollen required to produce one brood-cell, the pollen harvesting rate and compared our results with data for other specialized andrenid bee species. Pollen-foraging trips were registered and the activity events (entering, leaving or digging) recorded at the nests. The mean number of pollen-foraging trips per day was 5.3 and an average bee nest was active (and open) 88 min day–1. The bees were highly efficient in harvesting pollen and spent on average 10.7 min to complete one pollen-foraging trip. Most pollen-foraging trips (77%) were completed in less than 15 min. The duration of pollen-foraging trips increased over the day, presumably because pollen became more costly to harvest. Based on pollen counts (pollen loads on bees and pollen provisions) an average bee required 3.85 foraging trips to complete one brood cell and one bee managed to accomplish 1.37 brood cells in one day with suit- able weather. In the literature we found data on an additional 19 specialized andrenid bee species. Andrena humilis seems to be extremely efficient compared with most other species, with an average trip for pollen lasting almost one hour (average for andrenid bees = 46 min). An extremely low reproductive rate seems to be a common trait among specialized bees in the family Andrenidae with an average 0.9 offspring produced per day and less than ten offspring produced during the whole lifetime. The high degree of specialisation and the low reproductive rate among andrenid bees can explain the severe decline in many species today. Introduction in landscapes that provide access to multiple required resources (Michener & Rettenmeyer Most animals have to bridge some distances in 1956, Matheson et al. 1996). The more limited space and time to provide all resources neces- a resource becomes, the higher degree of spe- sary for survival, and many species only survive cialization is required to effectively utilize that This article has been scientifically edited by: Johan Kotze 406 Franzén & Larsson • ANN. ZOOL. FENNICI Vol. 44 rates in specialized andrenid bees. We studied the endangered and specialized solitary bee Andrena humilis Imhoff (Andrenidae). Our measurements included observations of daily bee activities, the rate of pollen harvested and the pollen required to produce one offspring. We expected the dura- tion of pollen-foraging trips to be negatively related to the time of day (when pollen becomes more costly to harvest), and female bees to differ in pollen harvesting efficiency. Our results were subsequently compared with studies of other Fig. 1. The distribution of Andrena humilis in Sweden. specialized andrenid bees. (a) until 1989 and (b) 1990–2007. Material and methods resource (Gillman & Crawley 1990). It is also advantageous to utilize a resource of high quality Study area and study species and to minimise the cost of travel (Mayr 1963, Plowright & Laverty 1984). Thus, time and This study was performed in Råshult, Sten- energy budgets are important to optimize while brohult parish in southern Sweden (56°37´N, collecting food, and therefore influence popula- 14°11´E). Råshult consists of ca. four hectares of tion survival, growth and reproduction (Stephens traditionally managed, dry meadows where the & Krebs 1986). Consequently, to maximize the pollen plant Leontodon hispidus occurs (Nils- number of offspring, foraging should be most son & Nilsson 2004). We studied the endan- efficient at times when food is abundant. gered solitary bee Andrena humilis, which is a Food resources in terms of nectar or pollen black, medium-sized bee (ca. 10 mm), special- limit the population size of many insects (Minck- ized on foraging pollen from species in the ley et al. 1994), and specialized solitary bees group Lactuceae (Asteraceae) (Westrich 1990). depend on abundant pollen resources (Larsson & In the study area this bee was observed to forage Franzén 2007). Most non-parasitic solitary bees pollen mainly from L. hispidus. In Sweden A. are obligate pollen consumers and often forage humilis have been reported to forage pollen from for pollen from a limited number of plant spe- Pilosella officinarum, L. hispidus and Hypoch- cies. Each single adult female bee constructs a oeris radicata (M. Larsson unpubl. data). This nest, gathers pollen from flowers and constructs bee species has probably matched its emergence separate brood cells for each egg. Pollen-forag- to the phenology of its pollen plant, as described ing females of solitary bees have evolved mor- in similar systems (Minckley et al. 1994, Minck- phological and behavioural adaptations to forage ley et al. 1999). It nests gregariously in the pollen efficiently (Wcislo et al. 1994, Herrera ground where vegetation is sparse or absent. 1996). Specialized solitary bees generally har- In Sweden, A. humilis has faced a dramatic vest pollen more efficiently on their preferred decline during the last 50 years and is red-listed pollen-plant than do generalist bees (Strickler as endangered (Gärdenfors 2005). Currently, A. 1979, 1982). Also, bees restricted to plant spe- humilis is known from less than 10 areas in cies where pollen is available only during a short southern Sweden (Fig. 1). period of time, have a particularly high pollen harvesting rate (Giovanetti & Lasso 2005). Many andrenid bees are declining and knowl- Nest observations edge about their foraging behaviour and repro- ductive rate are essential for the conservation A total of 450 nests were found in the study area of plant–pollinator systems. In this study we in 2005. The nests were found in three separate explored the foraging behaviour and reproductive aggregations on or close to sun-exposed path- ANN. ZOOL. FENNICI Vol. 44 • Pollen harvesting and reproductive rates in specialized solitary bees 407 ways extending through the hay meadows. We quantified as described for the pollen provision observed the bees at their nests in one of these samples. aggregations. The nest entrances were closed during the night but left opened during the day between the pollen-foraging trips. For each nest Statistical analyses observed, the observations started when the bee opened the nest entrance in the morning and The statistical analyses were based on data from continued until the nest was closed for the day. two days when the nests were observed from Each nest was uniquely labelled and one person opening until closed. A Generalised Linear could observe up to 20 nests simultaneously. On Mixed Model was used to test the duration (min) 21 June 2005 a pilot study was performed and of pollen-foraging trips in relation to the time (h) activities in 10 nests were observed. On 30 June of day and the nestcode (nestcode as a random 52 nests were labelled and observed by three per- factor, h as covariate). The time of day of nest sons and on 1 July 64 nests by four persons. The arrival (h) was categorized into periods of one nests were observed the entire day, from 08:00 hour. Tukey’s post hoc test was performed to test (before activity started) until activity ceased. for differences in hours of arrival. We were not For each nest we recorded the time for depar- able to re-identify and give the nests the same tures, arrivals and when digging occurred at the code as the day before, thus it was not possible entrance. Thirty-six observations were excluded to analyse day-effects correcting for the nest- from the statistical analyses as it was uncertain code. ANCOVA was used to test the number of at what time bees left or entered the nest. To be foraging trips (trips) of each female in one day in able to correct for possible temperature-related relation to the mean duration (min) of the pollen- effects, the temperature was measured each hour foraging trips, the activity length measured from between 9:00–13:00 on both days and the mean the time when the nest was open until closed per temperature for each day calculated. day (activity time) and the study day (study day used as a fixed factor, trips and activity time as covariates). Student’s t-test was used to see if Pollen samples there was any difference in the duration (min) of pollen-foraging trips and the number of forag- To quantify pollen provisions, nests of A. humi- ing trips (trips) during one day between the two lis were excavated. Fifteen cells that contained study days. Linear regression was used to relate pollen provisions with eggs were collected and the effect of the number of pollen-foraging trips preserved in 70% ethanol. In the laboratory, the per day to the mean duration of pollen-foraging provision samples were sonicated (KS101, Kerry trips. The relationship between the number of Ultrasonics Ltd.) for 35 min and quantified by pollen-foraging trips per day and the time when counting a known volume proportion of the the nest were opened and closed was analysed sample under a binocular microscope (the pro- using Pearson correlation.
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